Blender file Dialogue window always hides suggested folders, how to show by default?
I have tested this on Windows but I hope it works on Mac as well.
To modify Open File dialog settings, you need open new Blend, set the dialog panels to desired positions and save the current Blend as a Startup File:

Start the Blender so you have empty (default) project opened

Open the Open File dialog by File &gt; Open (or F1)

Resize your panels as you wish

Close the dialog so you return to Blender's workspace

Press Ctrl+U to Save Startup File - this saves the current settings as a default for any new projects (together with your panel)
(this trick also works for remembering startup window configuration for multiple displays)


Note: If you want to use F1 shortcut for opening a file, you need to configure this dialog as well, it's settings is independent from File -&gt; Open dialog.
To save settings of the Install Add-on dialog, don't open the dialog from User Preferences, but use Spacebar &amp; type &quot;Install&quot; &gt; hit Install Add-on from File. It will use Open File dialog settings this way.